Plasmodium falciparum-Infected erythrocytes and β-hematin induce partial maturation of human dendritic cells and increase their migratory ability in response to lymphoid chemokines

Infection and Immunity

Volumn 79, Issue 7, 2011, Pages 2727-2736

  Giusti, Pablo ^a   Urban, Britta C ^b,c   Frascaroli, Giada ^d   Albrecht, Letusa ^e   Tinti, Anna ^f   Troye Blomberg, Marita ^a   Varani, Stefania ^a,f,g  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^c Wellcome Trust/KEMRI Collaborative Programme   (Kenya)

^d UNIVERSITY OF ULM   (Germany)

^e KAROLINSKA INSTITUTE   (Sweden)

^f UNIVERSITY OF BOLOGNA   (Italy)

^g KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; BETA HEMATIN; CD83 ANTIGEN; CHEMOKINE; CHEMOKINE RECEPTOR CXCR4; HEMATIN; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANTIGEN EXPRESSION; ARTICLE; CELL MATURATION; CELL MIGRATION; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; ERYTHROCYTE; HUMAN; HUMAN CELL; MALARIA FALCIPARUM; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; T LYMPHOCYTE ACTIVATION;

ANTIGENS, CD; ANTIGENS, CD80; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINES; DENDRITIC CELLS; ERYTHROCYTES; HEMEPROTEINS; HUMANS; IMMUNOGLOBULINS; INTERLEUKIN-10; INTERLEUKIN-12; INTERLEUKIN-6; LYMPHOCYTE ACTIVATION; MEMBRANE GLYCOPROTEINS; PLASMODIUM FALCIPARUM; RECEPTORS, CXCR4; TUMOR NECROSIS FACTOR-ALPHA;

EID: 79959417317     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00649-10     Document Type: Article

References (50)

1. Ato, M., S. Stager, C. R. Engwerda, and P. M. Kaye. 2002. Defective CCR7 expression on dendritic cells contributes to the development of visceral leishmaniasis. Nat. Immunol. 3:1185-1191.
2. Banchereau, J., et al. 2000. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18:767-811.
3. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392:245-252.
4. Coban, C., et al. 2010. Immunogenicity of whole-parasite vaccines against Plasmodium falciparum involves malarial hemozoin and host TLR9. Cell Host Microbe 7:50-61.
5. Coban, C., K. J. Ishii, D. J. Sullivan, and N. Kumar. 2002. Purified malaria pigment (hemozoin) enhances dendritic cell maturation and modulates the isotype of antibodies induced by a DNA vaccine. Infect. Immun. 70:3939-3943.
6. Corrigan, R. A., and J. A. Rowe. 2010. Strain variation in early innate cytokine induction by Plasmodium falciparum. Parasite Immunol. 32:512-527.
7. Dostert, C., et al. 2009. Malarial hemozoin is a Nalp3 inflammasome activating danger signal. PLoS One 4:e6510.
8. Egan, T. J., E. Hempelmann, and W. W. Mavuso. 1999. Characterisation of synthetic beta-haematin and effects of the antimalarial drugs quinidine, halofantrine, desbutylhalofantrine and mefloquine on its formation. J. Inorg. Biochem. 73:101-107.
9. Egan, T. J., W. W. Mavuso, and K. K. Ncokazi. 2001. The mechanism of beta-hematin formation in acetate solution. Parallels between hemozoin formation and biomineralization processes. Biochemistry 40:204-213.
10. Elliott, S. R., et al. 2007. Inhibition of dendritic cell maturation by malaria is dose dependent and does not require Plasmodium falciparum erythrocyte membrane protein 1. Infect. Immun. 75:3621-3632.
11. Griffith, J. W., T. Sun, M. T. McIntosh, and R. Bucala. 2009. Pure hemozoin is inflammatory in vivo and activates the NALP3 inflammasome via release of uric acid. J. Immunol. 183:5208-5220.
12. Hanscheid, T., T. J. Egan, and M. P. Grobusch. 2007. Haemozoin: from melatonin pigment to drug target, diagnostic tool, and immune modulator. Lancet Infect. Dis. 7:675-685.
13. Inselburg, J., and H. S. Banyal. 1984. Plasmodium falciparum: synchronization of asexual development with aphidicolin, a DNA synthesis inhibitor. Exp. Parasitol. 57:48-54.
14. Jensen, J. B., and W. Trager. 1978. Plasmodium falciparum in culture: establishment of additional strains. Am. J. Trop. Med. Hyg. 27:743-746.
15. Keller, C. C., et al. 2004. Elevated nitric oxide production in children with malarial anemia: hemozoin-induced nitric oxide synthase type 2 transcripts and nitric oxide in blood mononuclear cells. Infect. Immun. 72:4868-4873.
16. Kotzor, N., M. Lechmann, E. Zinser, and A. Steinkasserer. 2004. The soluble form of CD83 dramatically changes the cytoskeleton of dendritic cells. Immunobiology 209:129-140.
17. Lambros, C., and J. P. Vanderberg. 1979. Synchronization of Plasmodium falciparum erythrocytic stages in culture. J. Parasitol. 65:418-420.
18. Langhorne, J., F. M. Ndungu, A. M. Sponaas, and K. Marsh. 2008. Immunity to malaria: more questions than answers. Nat. Immunol. 9:725-732.
19. Lechmann, M., et al. 2001. The extracellular domain of CD83 inhibits dendritic cell-mediated T cell stimulation and binds to a ligand on dendritic cells. J. Exp. Med. 194:1813-1821.
20. Leisewitz, A. L., et al. 2004. Response of the splenic dendritic cell population to malaria infection. Infect. Immun. 72:4233-4239.
21. Luft, T., et al. 2002. Functionally distinct dendritic cell (DC) populations induced by physiologic stimuli: prostaglandin E(2) regulates the migratory capacity of specific DC subsets. Blood 100:1362-1372.
22. Luty, A. J., et al. 2000. Low interleukin-12 activity in severe Plasmodium falciparum malaria. Infect. Immun. 68:3909-3915.
23. Lyke, K. E., et al. 2004. Serum levels of the proinflammatory cytokines interleukin-1 beta (IL-1beta), IL-6, IL-8, IL-10, tumor necrosis factor alpha, and IL-12(p70) in Malian children with severe Plasmodium falciparum malaria and matched uncomplicated malaria or healthy controls. Infect. Immun. 72:5630-5637.
24. Mellman, I., and R. M. Steinman. 2001. Dendritic cells: specialized and regulated antigen processing machines. Cell 106:255-258.
25. Millington, O. R., C. Di Lorenzo, R. S. Phillips, P. Garside, and J. M. Brewer. 2006. Suppression of adaptive immunity to heterologous antigens during Plasmodium infection through hemozoin-induced failure of dendritic cell function. J. Biol. 5:5.
26. Millington, O. R., et al. 2007. Malaria impairs T cell clustering and immune priming despite normal signal 1 from dendritic cells. PLoS Pathog. 3:1380-1387.
27. Mukherjee, P., and V. S. Chauhan. 2008. Plasmodium falciparum-free merozoites and infected RBCs distinctly affect soluble CD40 ligand-mediated maturation of immature monocyte-derived dendritic cells. J. Leukoc. Biol. 84:244-254.
28. Parroche, P., et al. 2007. Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc. Natl. Acad. Sci. U. S. A. 104:1919-1924.
29. Pichyangkul, S., et al. 2004. Malaria blood stage parasites activate human plasmacytoid dendritic cells and murine dendritic cells through a Toll-like receptor 9-dependent pathway. J. Immunol. 172:4926-4933.
30. Prakash, D., et al. 2006. Clusters of cytokines determine malaria severity in Plasmodium falciparum-infected patients from endemic areas of Central India. J. Infect. Dis. 194:198-207.
31. Riley, E. M., S. Wahl, D. J. Perkins, and L. Schofield. 2006. Regulating immunity to malaria. Parasite Immunol. 28:35-49.
32. Sallusto, F., and A. Lanzavecchia. 1994. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/ macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J. Exp. Med. 179:1109-1118.
33. Sallusto, F., et al. 1998. Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation. Eur. J. Immunol. 28:2760-2769.
34. Sanchez-Sanchez, N., L. Riol-Blanco, and J. L. Rodriguez-Fernandez. 2006. The multiple personalities of the chemokine receptor CCR7 in dendritic cells. J. Immunol. 176:5153-5159.
35. Schreibelt, G., et al. 2010. Toll-like receptor expression and function in human dendritic cell subsets: implications for dendritic cell-based anti-cancer immunotherapy. Cancer Immunol. Immunother. 59:1573-1582.
36. Skorokhod, O. A., M. Alessio, B. Mordmuller, P. Arese, and E. Schwarzer. 2004. Hemozoin (malarial pigment) inhibits differentiation and maturation of human monocyte-derived dendritic cells: a peroxisome proliferator-activated receptor-gamma-mediated effect. J. Immunol. 173:4066-4074.
37. Slater, A. F., et al. 1991. An iron-carboxylate bond links the heme units of malaria pigment. Proc. Natl. Acad. Sci. U. S. A. 88:325-329.
38. Sozzani, S., et al. 1997. Receptor expression and responsiveness of human dendritic cells to a defined set of CC and CXC chemokines. J. Immunol. 159:1993-2000.
39. Sponaas, A. M., et al. 2006. Malaria infection changes the ability of splenic dendritic cell populations to stimulate antigen-specific T cells. J. Exp. Med. 203:1427-1433.
40. Sullivan, D. J., Jr., I. Y. Gluzman, and D. E. Goldberg. 1996. Plasmodium hemozoin formation mediated by histidine-rich proteins. Science 271:219-222.
41. Tripathi, A. K., S. I. Khan, L. A. Walker, and B. L. Tekwani. 2004. Spectrophotometric determination of de novo hemozoin/beta-hematin formation in an in vitro assay. Anal. Biochem. 325:85-91.
42. Troye-Blomberg, M., H. Perlmann, M. E. Patarroyo, and P. Perlmann. 1983. Regulation of the immune response in Plasmodium falciparum malaria. II. Antigen specific proliferative responses in vitro. Clin. Exp. Immunol. 53:345-353.
43. Urban, B. C., et al. 2006. The frequency of BDCA3-positive dendritic cells is increased in the peripheral circulation of Kenyan children with severe malaria. Infect. Immun. 74:6700-6706.
44. Urban, B. C., et al. 1999. Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells. Nature 400:73-77.
45. Urban, B. C., et al. 2001. Peripheral blood dendritic cells in children with acute Plasmodium falciparum malaria. Blood 98:2859-2861.
46. Urban, B. C., and D. J. Roberts. 2003. Inhibition of T cell function during malaria: implications for immunology and vaccinology. J. Exp. Med. 197: 137-141.
47. van Helden, S. F., et al. 2006. A critical role for prostaglandin E2 in podosome dissolution and induction of high-speed migration during dendritic cell maturation. J. Immunol. 177:1567-1574.
48. Vogt, A. 2008. Selection of trophozoites by using magnetic cell sorting (MACS), p. 31-33. In K. Moll, I. Ljungström, H. Perlmann, A. Scherf, and M. Wahlgren (ed.), Methods in malaria research, 5th ed. MR4/ATCC, Manassas, VA.
49. World Health Organization. 2008. World malaria report 2008. World Health Organization, Geneva, Switzerland.
50. Wu, X., N. M. Gowda, S. Kumar, and D. C. Gowda. 2010. Protein-DNA complex is the exclusive malaria parasite component that activates dendritic cells and triggers innate immune responses. J. Immunol. 184:4338-4348